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Interactions between above- and belowground organisms modified in climate change experiments

Abstract

Climate change has been shown to affect ecosystem process rates1 and community composition2, with direct and indirect effects on belowground food webs3. In particular, altered rates of herbivory under future climate4 can be expected to influence above–belowground interactions5. Here, we use a multifactor, field-scale climate change experiment and independently manipulate atmospheric CO2 concentration, air and soil temperature and drought in all combinations since 2005. We show that changes in these factors modify the interaction between above- and belowground organisms. We use an insect herbivore to experimentally increase aboveground herbivory in grass phytometers exposed to all eight combinations of climate change factors for three years. Aboveground herbivory increased the abundance of belowground protozoans, microbial growth and microbial nitrogen availability. Increased CO2 modified these links through a reduction in herbivory and cascading effects through the soil food web. Interactions between CO2, drought and warming can affect belowground protozoan abundance. Our findings imply that climate change affects aboveground–belowground interactions through changes in nutrient availability.

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Figure 1: Effects of increased CO2 and herbivory on plant aboveground biomass.
Figure 2: Effects of aboveground herbivory and increased CO2 on belowground microbial biomass.
Figure 3: Limitation of microbial growth.
Figure 4: Effects of increased CO2 on above–belowground interactions.

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References

  1. Finzi, A. C. et al. Responses and feedbacks of coupled biogeochemical cycles to climate change: Examples from terrestrial ecosystems. Frontiers Ecol. Environ. 9, 61–67 (2011).

    Article  Google Scholar 

  2. Walther, G-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

    Article  CAS  Google Scholar 

  3. Eisenhauer, N., Cesarz, S., Koller, R., Worm, K. & Reich, P. B. Global change belowground: Impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob. Change Biol. 18, 435–447 (2012).

    Article  Google Scholar 

  4. Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008).

    Article  Google Scholar 

  5. Hillstrom, M., Meehan, T. D., Kelly, K. & Lindroth, R. L. Soil carbon and nitrogen mineralization following deposition of insect frass and greenfall from forests under elevated CO2 and O3 . Plant Soil 336, 75–85 (2010).

    Article  CAS  Google Scholar 

  6. Van der Putten, W. H et al. Empirical and theoretical challenges in aboveground–belowground ecology. Oecologia 161, 1–14 (2009).

    Article  Google Scholar 

  7. Norby, R. J., Warren, J. M., Iversen, C. M., Medlyn, B. E. & McMurtrie, R. E. CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc. Natl Acad. Sci. USA 107, 19368–19373 (2010).

    Article  CAS  Google Scholar 

  8. Reich, P. B. et al. Nitrogen limitation constrains sustainability of ecosystem response to CO2 . Nature 440, 922–925 (2006).

    Article  CAS  Google Scholar 

  9. Rustad, L. E. The response of terrestrial ecosystems to global climate change: towards an integrated approach. Sci. Total Environ. 404, 222–235 (2008).

    Article  CAS  Google Scholar 

  10. Antoninka, A. et al. Linking above- and belowground responses to global change at community and ecosystem scales. Glob. Change Biol. 15, 914–929 (2009).

    Article  Google Scholar 

  11. Johnson, S. N., Staley, J. T., Mcleod, F. A. L. & Hartley, S. E. Plant-mediated effects of soil invertebrates and summer drought on above-ground multitrophic interactions. J. Ecol. 99, 57–65 (2011).

    Article  Google Scholar 

  12. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S. & Vivanco, J. M. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233–266 (2006).

    Article  CAS  Google Scholar 

  13. Van der Putten, W. H. et al. Trophic interactions in a changing world. Basic Appl. Ecol. 5, 487–494 (2004).

    Article  Google Scholar 

  14. Bardgett, R. D. & Wardle, D. A. Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84, 2258–2268 (2003).

    Article  Google Scholar 

  15. Stiling, P. & Cornelissen, T. How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob. Change Biol. 13, 1823–1842 (2007).

    Article  Google Scholar 

  16. Post, E. & Pedersen, C. Opposing plant community responses to warming with and without herbivores. Proc. Natl Acad. Sci. USA 105, 12353–12358 (2008).

    Article  CAS  Google Scholar 

  17. Staley, J. T., Mortimer, S. R., Morecroft, M. D., Brown, V. K. & Masters, G. J. Summer drought alters plant-mediated competition between foliar- and root-feeding insects. Glob. Change Biol. 13, 866–877 (2007).

    Google Scholar 

  18. Mikkelsen, T. N. et al. Experimental design of multifactor climate change experiments with elevated CO2, warming and drought: The CLIMAITE project. Funct. Ecol. 22, 185–195 (2007).

    Google Scholar 

  19. De Graaff, M-A., Van Kessel, C. & Six, J. Rhizodeposition-induced decomposition increases N availability to wild and cultivated wheat genotypes under elevated CO2 . Soil Biol. Biochem. 41, 1094–1103 (2009).

    Article  CAS  Google Scholar 

  20. Tate, K. R. & Ross, D. J. Elevated CO2 and moisture effects on soil carbon storage and cycling in temperate grasslands. Glob. Change Biol. 3, 225–235 (1997).

    Article  Google Scholar 

  21. Larsen, K. S. et al. Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: Synthesizing results of the CLIMAITE project after two years of treatments. Glob. Change Biol. 17, 1884–1899 (2011).

    Article  Google Scholar 

  22. Finzi, A. C. et al. Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. Ecology 87, 15–25 (2006).

    Article  Google Scholar 

  23. Pineda, A., Zheng, S-j., Loon, J. J. A. V. & Dicke, M. Helping plants to deal with insects: The role of beneficial soil-borne microbes. Trends Plant Sci. 15, 507–514 (2010).

    Article  CAS  Google Scholar 

  24. Anderson, J. P. E. & Domsch, K. H. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol. Biochem. 10, 215–221 (1978).

    Article  CAS  Google Scholar 

  25. Wamberg, C., Christensen, S., Jakobsen, I., Muller, A. K. & Sorensen, S. J. The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol. Biochem. 35, 1349–1357 (2003).

    Article  CAS  Google Scholar 

  26. Scheu, S. Automated measurement of the respiratory response of soil microcompartments: Active microbial biomass in earthworm faeces. Soil Biol. Biochem. 24, 1113–1118 (1992).

    Article  Google Scholar 

  27. Ronn, R., Ekelund, F. & Christensen, S. Optimizing soil extract and broth media for MPN-enumeration of naked amoebae and heterotrophic flagellates in soil. Pedobiologia 39, 10–19 (1995).

    Google Scholar 

  28. Whitehead, A. G. & Hemming, J. R. A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann. Appl. Biol. 55, 25–38 (1965).

    Article  Google Scholar 

  29. Van Soest, P. J. Nutritional Ecology of the Ruminant 140–155 (Cornell Univ. Press, 1994).

    Google Scholar 

  30. R—A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2011); available at http://www.R-project.org.

Download references

Acknowledgements

We thank V. Kann Rasmussen Foundation (through the CLIMAITE project), Air Liquide and Dansk Olie og Naturgas energy for technical support. C.S. and D.G. were supported by the infrastructure ‘Increase’, financially supported by the European Union.

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K.S. and C.S. contributed equally to this manuscript. C.S., S.C. and C.B wrote the manuscript. K.S. and S.C. planned and initiated the study. K.S., D.G., C.S. and S.C. collected the data and had initial discussions of their implication. C.S. and S.C. carried out all statistical analyses. T.N.M. was in charge of the field study. All authors discussed the analysis and results and commented on the manuscript text.

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Correspondence to Christoph Scherber or David J. Gladbach.

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The authors declare no competing financial interests.

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Stevnbak, K., Scherber, C., Gladbach, D. et al. Interactions between above- and belowground organisms modified in climate change experiments. Nature Clim Change 2, 805–808 (2012). https://doi.org/10.1038/nclimate1544

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